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Abstract Coral reef sponges efficiently take up particulate and dissolved organic matter (DOM) from the water column and release compounds such as nucleosides, amino acids, and other dissolved metabolites to the surrounding reef via their exhalent seawater, but the influence of this process on reef picoplankton and nutrient processing is relatively unexplored. Here we examined the impact of sponge exhalent on the reef picoplankon community and subsequent alterations to the reef dissolved metabolite pool. We exposed reef picoplankton communities to a sponge exhalent water mixture (Niphates digitalis and Xestospongia muta) or filtered reef seawater (control) in closed, container-based dark incubations. We used 16S rRNA gene sequencing and flow cytometry-based cell counts to examine the picoplankton community and metabolomics and other analyses to examine the dissolved metabolite pool. The initial sponge exhalent was enriched in adenosine, inosine, chorismate, humic-like and amino acid-like components, and ammonium. Following 48 h of exposure to sponge exhalent, the picoplankton differed in composition, were reduced in diversity, showed doubled (or higher) growth efficiencies, and harbored increased copiotrophic and denitrifying taxa (Marinomonas, Pontibacterium, Aliiroseovarius) compared to control, reef-water based incubations. Alongside these picoplankton alterations, the sponge treatments, relative to seawater controls, had decreased adenosine, inosine, tryptophan, and ammonium, metabolites that may support the observed higher picoplankton growth efficiencies. Sponge treatments also had a net increase in several monosaccharides and other metabolites including anthranilate, riboflavin, nitrite, and nitrate. Our work demonstrates a link between sponge exhalent-associated metabolites and the picoplankton community, with exhalent water supporting an increased abundance of efficient, copiotrophic taxa that catabolize complex nutrients. The copiotrophic taxa were often different from those observed in previous algae and coral studies. These results have implications for better understanding the multifaceted role of sponges on picoplankton biomass with subsequent potential impacts to coral and other planktonic feeders in oligotrophic reef environments.

Abstract Coral reef biodiversity is maintained by a complex network of nutrient recycling among organisms. Sponges assimilate nutrients produced by other organisms like coral and algae, releasing them as particulate and dissolved matter, but to date, only a single trophic link between sponge-derived dissolved matter and a macroalgae has been identified. We sought to determine if sponge-coral nutrient exchange is reciprocal using a stable isotope ‘pulse-chase’ experiment to trace the uptake of 13C and 15N sponge-derived matter by the coral holobiont for three coral species (Acropora cervicornis, Orbicella faveolata, and Eunicea flexuosa). Coral holobionts incorporated 2.3–26.8x more 15N than 13C from sponge-derived matter and A. cervicornis incorporated more of both C and N than the other corals. Differential isotopic incorporation among coral species aligns with their ecophysiological characteristics (e.g., morphology, Symbiodiniaceae density). Our results elucidate a recycling pathway on coral reefs that has implications for improving coral aquaculture and management approaches.

Sponges are the richest source of bioactive organic small molecules, referred to as natural products, in the marine environment. It is well established that laboratory culturing-resistant symbiotic bacteria residing within the eukaryotic sponge host matrix often synthesize the natural products that are detected in the sponge tissue extracts. However, the contributions of the culturing-amenable commensal bacteria that are also associated with the sponge host to the overall metabolome of the sponge holobiont are not well defined. In this study, we cultured a large library of bacteria from three marine sponges commonly found in the Florida Keys. Metabolomes of isolated bacterial strains and that of the sponge holobiont were compared using mass spectrometry to reveal minimal metabolomic overlap between commensal bacteria and the sponge hosts. We also find that the phylogenetic overlap between cultured commensal bacteria and that of the sponge microbiome is minimal. Despite these observations, the commensal bacteria were found to be a rich resource for novel natural product discovery. Mass spectrometry-based metabolomics provided structural insights into these cryptic natural products. Pedagogic innovation in the form of laboratory curricula development is described which provided undergraduate students with hands-on instruction in microbiology and natural product discovery using metabolomic data mining strategies.

Abstract Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (

Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.

The pelagic Gulf of Mexico (GoM) is a complex system of dynamic physical oceanography (western boundary current, mesoscale eddies), high biological diversity, and community integration via diel vertical migration and lateral advection. Humans also heavily utilize this system, including its deep-sea components, for resource extraction, shipping, tourism, and other commercial activity. This utilization has had impacts, some with disastrous consequences. The Deepwater Horizon oil spill (DWHOS) occurred at a depth of ∼1500 m (Macondo wellhead), creating a persistent and toxic mixture of hydrocarbons and dispersant in the deep-pelagic (water column below 200 m depth) habitat. In order to assess the impacts of the DWHOS on this habitat, two large-scale research programs, described herein, were designed and executed. These programs, ONSAP and DEEPEND, aimed to quantitatively characterize the oceanic ecosystem of the northern GoM and to establish a time-series with which natural and anthropogenic changes could be detected. The approach was multi-disciplinary in nature and included in situ sampling, acoustic sensing, water column profiling and sampling, satellite remote sensing, AUV sensing, numerical modeling, genetic sequencing, and biogeochemical analyses. The synergy of these methodologies has provided new and unprecedented perspectives of an oceanic ecosystem with respect to composition, connectivity, drivers, and variability.

Oceanic diel vertical migration (DVM) constitutes the daily movement of various mesopelagic organisms migrating vertically from depth to feed in shallower waters and return to deeper water during the day. Accurate classification of taxa that participate in DVM remains non-trivial, and there can be discrepancies between methods. DEEPEND consortium (www.deependconsortium.org) scientists have been characterizing the diversity and trophic structure of pelagic communities in the northern Gulf of Mexico (nGoM). Profiling has included scientific echosounders to provide accurate and quantitative estimates of organismal density and timing as well as quantitative net sampling of micronekton. The use of environmental DNA (eDNA) can detect uncultured microbial taxa and the remnants that larger organisms leave behind in the environment. eDNA offers the potential to increase understanding of the DVM and the organisms that participate. Here we used real-time shipboard echosounder data to direct the sampling of eDNA in seawater at various time-points during the ascending and descending DVM. This approach allowed the observation of shifts in eDNA profiles concurrent with the movement of organisms in the DVM as measured by acoustic sensors. Seawater eDNA was sequenced using a high-throughput metabarcoding approach. Additionally, fine-scale acoustic data using an autonomous multifrequency echosounder was collected simultaneously with the eDNA samples and changes in organism density in the water column were compared with changes in eDNA profiles. Our results show distinct shifts in eukaryotic taxa such as copepods, cnidarians, and tunicates, over short timeframes during the DVM. These shifts in eDNA track changes in the depth of sound scattering layers (SSLs) of organisms and the density of organisms around the CTD during eDNA sampling. Dominant taxa in eDNA samples were mostly smaller organisms that may be below the size limit for acoustic detection, while taxa such as teleost fish were much less abundant in eDNA data compared to acoustic data. Overall, these data suggest that eDNA, may be a powerful new tool for understanding the dynamics and composition of the DVM, yet challenges remain to reconcile differences among sampling methodologies.

The Gulf of Mexico (GoM) is a dynamic marine ecosystem influenced by multiple natural and anthropogenic processes and inputs, such as the intrusion of warm oligotrophic water via the Loop Current, freshwater and nutrient input by the Mississippi River, and hydrocarbon inputs via natural seeps and industrial spills. Microbial plankton communities are important to pelagic food webs including in the GoM but understanding the drivers of the natural dynamics of these passively distributed microorganisms can be challenging in such a large and heterogeneous system. As part of the DEEPEND consortium, we applied high throughput 16S rRNA sequencing to investigate the spatial and temporal dynamics of pelagic microbial plankton related to several environmental conditions during two offshore cruises in 2015. Our results show dramatic community shifts across depths, especially between photic and aphotic zones. Though we only have two time points within a single year, observed temporal shifts in microbial plankton communities were restricted to the seasonally influenced epipelagic zone (0–200 m), and appear mainly driven by changes in temperature. Environmental selection in microbial plankton communities was depth-specific, with variables such as turbidity, salinity, and abundance of photosynthetic taxa strongly correlating with community structure in the epipelagic zone, while variables such as oxygen and specific nutrient concentrations were correlated with community structure at deeper depths.

Photosymbionts play an important role in the ecology and evolution of diverse host species within the marine environment. Although sponge-photosymbiont interactions have been well described from geographically disparate sites worldwide, our understanding of these interactions from shallow water systems within French Polynesia is limited. We surveyed diverse habitats around the north coast of Moorea, French Polynesia and screened sponges for the presence of photosymbionts. Overall sponge abundance and diversity were low, with

Recent studies have renewed interest in sponge ecology by emphasizing the functional importance of sponges in a broad array of ecosystem services. Many critically important habitats occupied by sponges face chronic stressors that might lead to alterations in their diversity, relatedness, and functional attributes. We addressed whether proximity to human activity might be a significant factor in structuring sponge community composition, as well as potential functional roles, by monitoring sponge diversity and abundance at two structurally similar sites that vary in distance to areas of high coastal development in Bocas Del Toro, Panama. We surveyed sponge communities at each site using belt transects and differences between two sites were compared using the following variables: (1) sponge species richness, Shannon diversity, and inverse Simpson’s diversity; (2) phylogenetic diversity; (3) taxonomic and phylogenetic beta diversity; (4) trait diversity and dissimilarity; and (5) phylogenetic and trait patterns in community structure. We observed significantly higher sponge diversity at Punta Caracol, the site most distant from human development (∼5 km). Although phylogenetic diversity was lower at Saigon Bay, the site adjacent to a large village including many houses, businesses, and an airport, the sites did not exhibit significantly different patterns of phylogenetic relatedness in species composition. However, each site had a distinct taxonomic and phylogenetic composition (beta diversity). In addition, the sponge community at Saigon included a higher relative abundance of sponges with high microbial abundance and high chlorophyll a concentration, whereas the community at Punta Caracol had a more even distribution of these traits, yielding a significant difference in functional trait diversity between sites. These results suggest that lower diversity and potentially altered community function might be associated with proximity to human populations. This study highlights the importance of evaluating functional traits and phylogenetic diversity in addition to common diversity metrics when assessing potential environmental impacts on benthic communities.

Hosting symbionts provides many eukaryotes with access to the products of microbial metabolism that are crucial for host performance. On tropical coral reefs, many (High Microbial Abundance [HMA]) but not all (Low Microbial Abundance [LMA]) marine sponges host abundant symbiont communities. Although recent research has revealed substantial variation in these sponge-microbe associations (termed holobionts), little is known about the ecological implications of this diversity. We investigated the expansion of diverse sponge species across isotopic niche space by calculating niche size (as standard ellipse area [SEAc]) and assessing the relative placement of common sponge species in bivariate (δ13C and δ15N) plots. Sponges for this study were collected from the relatively isolated reefs within the Miskito Cays of Honduras. These reefs support diverse communities of HMA and LMA species that together span a gradient of photosymbiont abundance, as revealed by chlorophyll a analysis. HMA sponges occupied unique niche space compared to LMA species, but the placement of some HMA sponges was driven by photosymbiont abundance. In addition, photosymbiont abundance explained a significant portion of the variation in isotope values, suggesting that access to autotrophic metabolism provided by photosymbionts is an important predictor in the location of species within isotopic space. Host identity accounted for over 70% of the variation in isotope values within the Miskito Cays and there was substantial variation in the placement of individual species within isotopic niche space, suggesting that holobiont metabolic diversity may allow taxonomically diverse sponge species to utilize unique sources of nutrients within a reef system. This study provides initial evidence that microbial symbionts allow sponges to expand into novel physiochemical niche space. This expansion may reduce competitive interactions within coral reefs and promote diversification of these communities.

Deep-sea anglerfishes are relatively abundant and diverse, but their luminescent bacterial symbionts remain enigmatic. The genomes of two symbiont species have qualities common to vertically transmitted, host-dependent bacteria. However, a number of traits suggest that these symbionts may be environmentally acquired. To determine how anglerfish symbionts are transmitted, we analyzed bacteria-host codivergence across six diverse anglerfish genera. Most of the anglerfish species surveyed shared a common species of symbiont. Only one other symbiont species was found, which had a specific relationship with one anglerfish species, Cryptopsaras couesii. Host and symbiont phylogenies lacked congruence, and there was no statistical support for codivergence broadly. We also recovered symbiont-specific gene sequences from water collected near hosts, suggesting environmental persistence of symbionts. Based on these results we conclude that diverse anglerfishes share symbionts that are acquired from the environment, and that these bacteria have undergone extreme genome reduction although they are not vertically transmitted.

Marine diseases are of increasing concern for coral reef ecosystems, but often their causes, dynamics and impacts are unknown. The current study investigated the epidemiology of Aplysina Red Band Syndrome (ARBS), a disease affecting the Caribbean sponge Aplysina cauliformis, at both the individual and population levels. The fates of marked healthy and ARBS-infected sponges were examined over the course of a year. Population-level impacts and transmission mechanisms of ARBS were investigated by monitoring two populations of A. cauliformis over a three year period using digital photography and diver-collected data, and analyzing these data with GIS techniques of spatial analysis. In this study, three commonly used spatial statistics (Ripley's K, Getis-Ord General G, and Moran's Index) were compared to each other and with direct measurements of individual interactions using join-counts, to determine the ideal method for investigating disease dynamics and transmission mechanisms in this system. During the study period, Hurricane Irene directly impacted these populations, providing an opportunity to assess potential storm effects on A. cauliformis and ARBS.Infection with ARBS caused increased loss of healthy sponge tissue over time and a higher likelihood of individual mortality. Hurricane Irene had a dramatic effect on A. cauliformis populations by greatly reducing sponge biomass on the reef, especially among diseased individuals. Spatial analysis showed that direct contact between A. cauliformis individuals was the likely transmission mechanism for ARBS within a population, evidenced by a significantly higher number of contact-joins between diseased sponges compared to random. Of the spatial statistics compared, the Moran's Index best represented true connections between diseased sponges in the survey area. This study showed that spatial analysis can be a powerful tool for investigating disease dynamics and transmission in a coral reef ecosystem.